Nitric oxide system and protein nitration are modified by an acute hypobaric hypoxia in the adult rat hippocampus

Journal of Neuropathology and Experimental Neurology

Volumn 62, Issue 8, 2003, Pages 863-877

  Encinas, Juan Manuel ^b   Serrano, Julia ^b   Bentura, Maria Luisa ^b   Castro Blanco, Susana ^b   Fernández, Ana Patricia ^b   Rodrigo, José ^a  

^a INSTITUTO CAJAL   (Spain)

^b NONE

Author keywords

Hippocampus; Hypobaric hypoxia; Nitric oxide; Protein nitration

Indexed keywords

3 NITROTYROSINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN;

ALTITUDE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; HIPPOCAMPUS; HYPOBARISM; HYPOXIA; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; MALE; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PYRAMIDAL NERVE CELL; RAT; REOXYGENATION;

EID: 0041833551     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/62.8.863     Document Type: Article

References (77)

1. Bahrke M, Shukitt-Hale B. Effects of Altitude on Mood, behaviour and Cognitive Functioning. Sports medicine 1993;16:97-125
2. Pulsinelli WA. Selective neuronal vulnerability: Morphological and molecular characteristics. Prog Brain Res 1985;63:29-37
3. Cervos-Navarro J, Diemer NH. Selective vulnerability in brain hypoxia. Crit Rev Neurobiol 1991;6:149-82
4. Trouvin JH, Prioux-Guyonneau M, Cohen Y, Jacquot C. Rat brain monoamine metabolism and hypobaric hypoxia: A new approach. Gen Pharmacol 1986;17:69-73
5. Pichiule P, Chavez JC, Boero J, Arregui A. Chronic hypoxia induces modification of the N-methyl-D-aspartate receptor in rat brain. Neurosci Lett 1996;218:83-86
6. Zamorskii II, Pishak VP. Effect of melatonin on cyclic nucleotide content and intensity of lipid peroxidation in the hippocampus and habenula of rats exposed to acute hypoxia. Bull Exp Biol Med 2000;130:756-58
7. Medico M, De Vivo S, Tomasello C, et al. Behavioral and neurochemical effects of dopaminergic drugs in models of brain injury. Eur Neuropsychopharmacol 2002;12:187-94
8. Krapivin SV, Romanova VE, Voronina TA, Luk'ianova LD. An electrophysiological study of the brain of rats with different resistances to oxygen deficiency in acute hypoxia. Fiziol Zh SSSR Im I M Sechenova 1991;77:1-6
9. Shukitt-Hale B, Kadar T, Marlowe BE, et al. Morphological alterations in the hippocampus following hypobaric hypoxia. Hum Exp Toxicol 1996;15:312-19
10. Kadar T, Dachir S, Shukitt-Hale B, Levy A. Sub-regional hippocampal vulnerability in various animal models leading to cognitive dysfunction. J Neural Transm 1998;105:987-1004
11. Boero JA, Ascher J, Arregui A, Rovainen C, Woolsey TA. Increased brain capillaries in chronic hypoxia. J Appl Physiol 1999;86:1211-19
12. Pagani M, Ansjon R, Lind F, et al. Effects of acute hypobaric hypoxia on regional cerebral blood flow distribution: A single photon emission computed tomography study in humans. Acta Physiol Scand 2000;168:377-83
13. Regard M, Oelz O, Brugger P, Landis T. Persistent cognitive impairment in climbers after repeated exposure to extreme altitude. Neurology 1989;39:210-13
14. Cavaletti G, Tredici G. Long-lasting neuropsychological changes after a single high altitude climb. Acta Neurol Scand 1993;87:103-5
15. Shukitt-Hale B, Stillman MJ, Welch DI, Levy A, Devine JA, Lieberman HR. Hypobaric hypoxia impairs spatial memory in an elevation-dependent fashion. Behav Neural Biol 1994;6:244-52
16. Beckman JS. The double-edged role of nitric oxide in brain function and superoxide-mediated injury. J Dev Physiol 1991;15:53-59
17. Malinski T, Bailey F, Zhang ZG, Chopp M. Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 1993;13:355-58
18. Iadecola C. Bright and dark sides of nitric oxide in ischemic brain injury. Neuroscience 1997;20:132-39
19. Rodrigo J, Alonso D, Fernández AP, et al. Neuronal and inducible nitric oxide synthase expression and protein nitration in rat cerebellum after oxygen and glucose deprivation. Brain Res 2001;909:20-45
20. Alonso D, Serrano J, Rodriguez I, et al. Effects of oxygen and glucose deprivation on the expression and distribution of neuronal and inducible nitric oxide synthases and on protein nitration in rat cerebral cortex. J Comp Neurol 2002;443:183-200
21. Matsuoka Y, Kitamura Y, Tooyama I, Kimura H, Taniguchi T. In vivo hypoxia-induced neuronal damage with an enhancement of neuronal nitric oxide synthase immunoreactivity in hippocampus. Exp Neurol 1997;146:57-66
22. Malyshev IY, Zenina TA, Golubeva LY, et al. NO-dependent mechanisms of adaptation to hypoxia. Nitric Oxide 1999;3:105-13
23. Prabhakar NR, Pieramici SF, Premkumar DR, Kumar GK, Kalaria RN. Activation of nitric oxide synthase gene expression by hypoxia in central and peripheral neurons. Brain Res Mol Brain Res 1996;43:341-46
24. Luo Y, Kaur C, Ling EA. Hypobaric hypoxia induces fos and neuronal nitric oxide synthase expression in the paraventricular and supraoptic nucleus in rats. Neurosci Lett 2000;296:145-48
25. Palmer RMJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327:524-26
26. Forstermann U, Schmidt HW, Pollock JS, et al. Isoforms of nitric oxide synthase. Characterization and purification from different cell types. Biochem Pharmacol 1991;42:1849-57
27. Marletta MA, Yoon PS, Iyengar R, Leaf CD, Wishnok JS. Macrophage oxidation of L-arginine to nitrite and nitrate: Nitric oxide is an intermediate. Biochemistry 1988;27:8706-11
28. Szabo C, Thiemermann C. Regulation of the expression of the inducible isoform of nitric oxide synthase. Adv Pharmacol 1995;34:113-53
29. Moro MA, De Alba J, Leza JC, et al. Neuronal expression of inducible nitric oxide synthase after oxygen and glucose deprivation in rat forebrain slices. Eur J Neurosci 1998;10:445-56
30. Uttenthal LO, Alonso D, Fernandez AP, et al. Neuronal and inducible nitric oxide synthase and nitrotyrosine immunoreactivities in the cerebral cortex of the aging rat. Microsc Res Tech 1998;43:75-88
31. Valtschanoff JG, Weinberg RJ, Kharazia VN, Nakane M, Schmidt HH. Neurons in rat hippocampus that synthesize nitric oxide. J Comp Neurol 1993;331:111-21
32. Szabo C. Physiological and pathophysiological roles of nitric oxide in the central nervous system. Brain Res Bull 1996;41:131-41
33. Kelly PA, Ritchie IM, Arbuthnott GW. Inhibition of neuronal nitric oxide synthase by 7-nitroindazole: Effects upon local cerebral blood flow and glucose use in the rat. J Cereb Blood Flow Metab 1995;15:766-73
34. Huang PL, Huang Z, Mashimo H, et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 1995;377:239-42
35. Koppenol WH, Moreno JJ, Pryor WA, Ischiropoulos H, Beckman JS. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem Res Toxicol 1992;5:834-42
36. Pryor WA, Squadrito GL. The chemistry of peroxynitrite: A product from the reaction of nitric oxide with superoxide. Am J Physiol 1995;268:L699-L722
37. Beckman JS, Koppenol WH. Nitric oxide, superoxide and peroxynitrite: The good, the bad, and the ugly. Am J Physiol 1996;271:1424-37
38. Ischiropoulos H, Zhu L, Chen J, et al. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys 1992;298:431-37
39. Ischiropoulos H, al-Mehdi AB. Peroxynitrite-mediated oxidative protein modifications. FEBS Lett 1995;364:279-82
40. Alonso D, Encinas JM, Uttenthal LO, Bosca L, et al. Coexistence of translocated cytochrome c and nitrated protein in neurons of the rat cerebral cortex after oxygen and glucose deprivation. Neuroscience 2002;111:47-56
41. Rodrigo J, Springall DR, Uttenthal O, et al. Localization of nitric oxide synthase in the adult rat brain. Philos Trans R Soc Lond B Biol. Sci 1994;345:175-221
42. Shu S, Ju G, Fan L. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 1988;85:169-71
43. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54
44. Radomski MW, Vallance PJ, Whitely G, Foxwell N, Moncada S. Modulation of platelet adhesion to human vascular endothelium by the constitutive and cytokine-inducible nitric oxide synthases. Cardiovasc Res 1993;27:1380-82
45. Bohme GA, Bon C, Stutzmann JM, Doble A, Blanchard JC. Possible involvement of nitric oxide in long-term potentiation. Eur J Pharmacol 1991;199:379-81
46. Schuman EM, Madison DV. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 1991;254:1503-6
47. Mizutani A, Saito H, Abe K. Involvement of nitric oxide in long-term potentiation in the dentate gyrus in vivo. Brain Res 1993;605:309-11
48. Bohme GA, Bon C, Lemaire M, Reibaud M, Piot O, Stutzmann JM, Doble A, Blanchard JC. Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats. Proc Natl Acad Sci USA 1993;90:9191-94
49. Estall LB, Grant SJ, Cicala GA. Inhibition of nitric oxide (NO) production selectively impairs learning and memory in the rat. Pharmacol Biochem Behav 1993;46:959-62
50. Ohno M, Yamamoto T, Watanabe S. Deficits in working memory following inhibition of hippocampal nitric oxide synthesis in the rat. Brain Res 1993;632:36-40
51. Beasley TC, Bari F, Thore C, Thrikawala N, Louis T, Busija D. Cerebral ischemia/reperfusion increases endothelial nitric oxide synthase levels by an indomethacin-sensitive mechanism. J Cereb Blood Flow Metab 1998;18:88-96
52. Robertson SC, Loftus CM. Effect of N-methyl-D-aspartate and inhibition of neuronal nitric oxide on collateral cerebral blood flow after middle cerebral artery occlusion. Neurosurgery 1998;42:117-24
53. Holscher C, McGlinchey L, Anwyl R, Rowan MJ. 7-Nitro indazole, a selective neuronal nitric oxide synthase inhibitor in vivo, impairs spatial learning in the rat. Learn Mem 1996;2:267-78
54. Dere E, Frisch C, De Souza Silva MA, Godecke A, Schrader J, Huston JP. Unaltered radial maze performance and brain acetylcholine of the endothelial nitric oxide synthase knockout mouse. Neuroscience 2001;107:561-70
55. Trifiletti RR. Neuroprotective effects of NG-nitro-L-arginine in focal stroke in the 7-day old rat. Eur J Pharmacol 1992;218:197-98
56. Eliasson MJ, Huang Z, Ferrante RJ, et al. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J Neurosci 1999;19:5910-18
57. Caldwell M, O'Neill M, Earley B, Leonard B. NG-Nitro-L-arginine protects against ischaemia-induced increases in nitric oxide and hippocampal neuro-degeneration in the gerbil. Eur J Pharmacol 1994;260:191-200
58. O'Neill MJ, Hicks C, Ward M. Neuroprotective effects of 7-nitroindazole in the gerbil model of global cerebral ischaemia. Eur J Pharmacol 1996;310:115-22
59. Sasaki T, Hamada J, Shibata M, Araki N, Fukuuchi Y. Inhibition of nitric oxide production during global ischemia ameliorates ischemic damage of pyramidal neurons in the hippocampus. Keio J Med 2001;50:182-87
60. Zhang F, Iadecola C. Nitroprusside improves blood flow and reduces brain damage after focal ischemia. Neuroreport 1993;4:559-62
61. Bolanos JP, Almeida A. Roles of nitric oxide in brain hypoxia-ischemia. Biochim Biophys Acta 1999;1411:415-36
62. Kader A, Frazzini VI, Solomon RA, Trifiletti RR. Nitric oxide production during focal cerebral ischemia in rats. Stroke 1993;24:1709-16
63. Cazevieille C, Muller A, Meynier F, Bonne C. Superoxide and nitric oxide cooperation in hypoxia/reoxygenation-induced neuron injury. Free Radic Biol Med 1993;14:389-95
64. Samdani AF, Dawson TM, Dawson VL. Nitric oxide synthase in models of focal ischemia. Stroke 1997;28:1283-88
65. Zhang ZG, Chopp M, Zaloga C, Pollock JS, Forstermann U. Cerebral endothelial nitric oxide synthase expression after focal cerebral ischemia in rats. Stroke 1993;24:2016-22
66. Minc-Golomb D, Tsarfaty I, Schwartz JP. Expression of inducible nitric oxide synthase by neurones following exposure to endotoxin and cytokine. Br J Pharmacol 1994;112:720-22
67. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 1995;182:1683-93
68. Yin K, Juurlink BH. Regulation of expression of nuclear factor kappa B RelA in oligodendrocytes: Effect of hypoxia. Neuroreport 2000;11:1877-81
69. Iadecola C, Zhang F, Casey R, Nagayama M, Ross ME. Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 1997;17:9157-64
70. Iadecola C, Zhang F, Casey R, Clark HB, Ross ME. Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke 1996;27:1373-80
71. Forster C, Clark HB, Ross ME, Iadecola C. Inducible nitric oxide synthase expression in human cerebral infarcts. Acta Neuropath 1999;97:215-20
72. Daval JL, Ghersi-Egea JF, Oillet J, Koziel V. A simple method for evaluation of superoxide radical production in neural cells under various culture conditions: Application to hypoxia. Cereb Blood Flow Metab 1995;15:71-77
73. Forman LJ, Liu P, Nagele RG, Yin K, Wong PY. Augmentation of nitric oxide, superoxide, and peroxynitrite production during cerebral ischemia and reperfusion in the rat. Neurochem Res 1998;23:141-48
74. Van-der-Vliet A, Smith D, O'Neill CA, et al. Interactions of peroxynitrite with human plasma and its constituents: oxidative damage and antioxidant depletion. Biochem J 1994;303:295-301
75. Bolan EA, Gracy KN, Chan J, Trifiletti RR, Pickel VM. Ultrastructural localization of nitrotyrosine within the caudate-putamen nucleus and the globus pallidus of normal rat brain. J Neurosci 2000;20:4798-4808
76. Tanaka K, Shirai T, Nagata E, Dembo T, Fukuuchi Y. Immunohistochemical detection of nitrotyrosine in postischemic cerebral cortex in gerbil. Neurosci Lett 1997;235:85-88
77. Radi R, Denicola A, Alvarez B, Ferrer-Sueta G, Rubbo H. The biological chemistry of peroxynitrite. In: Ignarro LJ, ed. Nitric oxide. Biology and pathobiology. San Diego: Academic Press, 2000:57-83